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Epigenetic Responses of Hare Barley (Hordeum Murinum Subsp. Leporinum) to Climate Change: an Experimental, Trait-Based Approach

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Epigenetic Responses of Hare Barley (Hordeum Murinum Subsp. Leporinum) to Climate Change: an Experimental, Trait-Based Approach Heredity (2021) 126:748–762 https://doi.org/10.1038/s41437-021-00415-y ARTICLE Epigenetic responses of hare barley (Hordeum murinum subsp. leporinum) to climate change: an experimental, trait-based approach 1,2,3 2 1 2 Víctor Chano ● Tania Domínguez-Flores ● Maria Dolores Hidalgo-Galvez ● Jesús Rodríguez-Calcerrada ● Ignacio Manuel Pérez-Ramos1 Received: 12 June 2020 / Revised: 29 January 2021 / Accepted: 29 January 2021 / Published online: 19 February 2021 © The Author(s) 2021. This article is published with open access Abstract The impact of reduced rainfall and increased temperatures forecasted by climate change models on plant communities will depend on the capacity of plant species to acclimate and adapt to new environmental conditions. The acclimation process is mainly driven by epigenetic regulation, including structural and chemical modifications on the genome that do not affect the nucleotide sequence. In plants, one of the best-known epigenetic mechanisms is cytosine-methylation. We evaluated the impact of 30% reduced rainfall (hereafter “drought” treatment; D), 3 °C increased air temperature (“warming”; W), and the combination of D and W (WD) on the phenotypic and epigenetic variability of Hordeum murinum subsp. leporinum L., 1234567890();,: 1234567890();,: a grass species of high relevance in Mediterranean agroforestry systems. A full factorial experiment was set up in a savannah-like ecosystem located in southwestern Spain. H. murinum exhibited a large phenotypic plasticity in response to climatic conditions. Plants subjected to warmer conditions (i.e., W and WD treatments) flowered earlier, and those subjected to combined stress (WD) showed a higher investment in leaf area per unit of leaf mass (i.e., higher SLA) and produced heavier seeds. Our results also indicated that both the level and patterns of methylation varied substantially with the climatic treatments, with the combination of D and W inducing a clearly different epigenetic response compared to that promoted by D and W separately. The main conclusion achieved in this work suggests a potential role of epigenetic regulation of gene expression for the maintenance of homoeostasis and functional stability under future climate change scenarios. Introduction There is a growing interest in understanding how plants will adapt to the projected changes in climate. Plant species respond to environmental changes by means of multiple Supplementary information The online version contains morphological and physiological adjustments that serve to supplementary material available at https://doi.org/10.1038/s41437- alleviate stress levels and to increase the uptake of limiting 021-00415-y. resources (Nicotra et al. 2010;Freschetetal.2018;Pérez- * Víctor Chano Ramos et al. 2019). For example, plants subjected to [email protected] greater water/nutrient limitations usually exhibit a suite of trait values associated to efficient resource conservation 1 Research Group “Sistemas Forestales Mediterráneos”, Instituto de Recursos Naturales y Agrobiología de Sevilla. Dpto, use (e.g., plants with small-sized and high-density leaves) Biogeoquímica, Ecología Vegetal y Microbiana, Consejo Superior (Chapin et al. 1993;Wrightetal.2004), which increases de Investigaciones Científicas, Av. Reina Mercedes 10, 41012 competitive abilities under resource-limiting conditions. Sevilla, Spain This strategy contrasts with that displayed by plants 2 Research Group “Sistemas Naturales e Historia Forestal”, ETSI inhabiting moist and fertile sites, with opposite trait values Montes, Forestal y del Medio Natural. Dpto, Sistemas y Recursos related to a rapid return on investment. Moreover, under Naturales, Universidad Politécnica de Madrid, Ciudad Universitaria s/n, 28040 Madrid, Spain non-limiting conditions of soil water and nutrient avail- 3 ability, an increase in air temperature could result in Present address: Department of Forest Genetics and Forest Tree fi Breeding, University of Göttingen, Büsgenweg 2, 37077 thinner leaves with higher speci c leaf area that favour Göttingen, Germany plant carbon uptake and growth (Poorter et al. 2009; Epigenetic responses of hare barley (Hordeum murinum subsp. leporinum) to climate change: an. 749 Lamaouietal.2018). Plants can also modify their repro- natural populations differing in a limited (one or two) ductive output and phenology under different environ- number of factors. However, in nature, plants are exposed to mental scenarios of temperature and resource limitation a variety of constraints, which constitute a multidimensional (Valencia et al. 2016; Pérez-Ramos et al. 2020). space where many factors act simultaneously and inter- The species’ ability to vary its phenotypic expression actively (Ibáñez and Schupp 2001; Gómez 2004). Since the across environments is mainly driven by genetic variability, effect of one stress factor on plant performance may be which is in turn originated by sexual reproduction and exacerbated or mitigated by another (Mitchell et al. 2015), random mutations (Ewens 2013). In addition, there are the impact of a combination of various stress factors may evidences that epigenetic processes (i.e., structural and differ from the sum of the impacts caused by each factor chemical modifications on the genome that do not affect the applied individually. As a result, combined stress factors nucleotide sequence) can promote fast and reversible phe- may enhance phenotypic variation and plant fitness despite notypic variations in response to environmental changes the presumably higher costs of plasticity (Lampei 2019). (Bossdorf et al. 2008). These epigenetic mechanisms act in Therefore, an accurate prediction of climate change pro- a switch mode, activating/deactivating gene transcription in jections on plant phenotypic variability requires the con- three different ways: (i) DNA methylation by the covalent sideration of potential additive and interactive effects of binding of methyl groups to cytosine nucleotides (5 mC), different abiotic factors. (ii) regulation of DNA accessibility by histone modification The role of methylation or demethylation processes in and (iii) post-transcriptional regulation by non-coding response to stress has not been fully elucidated and seems to RNAs activity such as microRNAs (Bossdorf et al. 2008). be dynamic in time (Liu et al. 2018). For instance, several In plants, DNA methylation has been found to silence alleles were identified and related to a plastic response to transposable elements (TEs) and gene expression (Bartels climate variation in natural populations of Arabidopsis et al. 2018), with promoter methylated genes having lower thaliana, with diverse genome-wide methylation patterns transcription levels (Zhang et al. 2006; Li et al. 2012). associated to seasonality (Shen et al. 2014). Wang et al. Recent studies have argued that epigenetic mechanisms (2011) detected different patterns of genome-wide methy- could play a relevant role in microevolution under chal- lation/demethylation in rice induced by water limitation, lenging environmental scenarios, such as those promoted by with plants exhibiting 70% reversibility to the original climate change (e.g., Kronholm et al. 2017; Jeremias et al. status after drought cessation. Another study also detected 2018; Münzbergová et al. 2019). In fact, although it is drought-induced responses in rice, with hyper- and hypo- broadly assumed that species with high genetic variability methylation being related to susceptibility and tolerance to have higher adaptation potential for a larger variety of water deficit, respectively (Gayacharan 2013). On the environmental conditions than species with low genetic other hand, DNA-methylation processes have been widely diversity (Anderson et al. 2011), recent studies (e.g., Zhang studied in response to heat stress, especially through the et al. 2016) have demonstrated the importance of epigenetic activity of methyltransferases (see review by Liu et al. diversity for environmental adaptation in plant species 2015). All these studies suggest that methylation patterns in with limited genetic diversity. Notwithstanding, there are response to stress conditions depend on the source of stress, still many gaps on the role of epigenetics as a driver of as well as on the genotype, the tissue and the ontogeny this source of phenotypic variability across contrasted (Bonasio et al. 2010; Tan 2010; Wang et al. 2011; Mastan environments. et al. 2012), and that these factors will likely encompass a Several studies have reported the influence of epigenetic wide range of responsive genes. responses to different environmental conditions on some In the present study we analysed the two main sources of developmental processes. For instance, it has been demon- genotypic variability (i.e., genetic and epigenetic) of an strated that phenotypic variations in Viola cazorlensis and annual grass species dominant in Mediterranean savannah- allopolyploid orchids in response to climate are mediated by like ecosystems, Hordeum murinum subsp. leporinum L. both genetic and epigenetic processes (Herrera and Bazaga (hare barley, hereafter), with great relevance in pasture 2010; Paun et al. 2010). Other works have also focused on dynamics due to its fast growth and high palatability for the epigenetic responses to different sources of stress, both livestock (Hulting and Haavisto 2013). This species is biotic, such as herbivory, disease or plant competition for widely distributed in Europe and Middle East and has been nutrients (Conrath et al. 2002;
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